Population Genomics Provides Key Insights in Ecology and Evolution

  • Paul A. HohenloheEmail author
  • Brian K. Hand
  • Kimberly R. Andrews
  • Gordon Luikart
Part of the Population Genomics book series (POGE)


Population genomic tools have revolutionized many aspects of biology, as detailed throughout the chapters of this volume. In particular, population genomics has provided key insights into ecological and evolutionary processes in natural and managed populations. These studies address a wide range of questions, including demography, phylogeny, genetics of ecologically relevant traits, and adaptation. They have also facilitated the conservation and management of biodiversity and harvested populations. Rather than exhaustively document the applications of population genomics in ecology and evolution, in this chapter we provide perspectives on a few key issues confronting researchers seeking to use population genomic tools in non-model systems. A wide variety of molecular and computational genomic approaches are available and have been used in ecological and evolutionary studies. There is no single best approach; rather, the genomic approach used should be tailored to best address the particular study goals and guided by the biology of the system. A large number of trade-offs, costs, and benefits distinguish genomic approaches, which we discuss below. To illustrate these issues, we focus on several published case studies and assess how the research questions were addressed.


Genetics of adaptation Inbreeding Next-generation sequencing Phylogenomics Population genetic structure Population genomics 



PAH and KRA received support from NSF grant DEB-1316549. BKH was partially supported by funds from NSF grant DOB-1639014 and NASA NNX14AB84G. KRA was supported by the University of Idaho College of Natural Resources, USA. This is PMEL contribution number 4750 and Joint Institute for the Study of the Atmosphere and Ocean (JISAO) and NOAA Cooperative Agreement and NA15OAR4320063, contribution number 2018-0135.


  1. Ali OA, O’Rourke SM, Amish SJ, Meek MH, Luikart G, Jeffres C, Miller MR. RAD capture (rapture): flexible and efficient sequence-based genotyping. Genetics. 2016;202:389–400.PubMedGoogle Scholar
  2. Allendorf FW. Genetics and the conservation of natural populations: allozymes to genomes. Mol Ecol. 2017;26:420–30.PubMedGoogle Scholar
  3. Allendorf FW, Hohenlohe PA, Luikart G. Genomics and the future of conservation genetics. Nat Rev Genet. 2010;11:697–709.PubMedGoogle Scholar
  4. Amish SJ, Hohenlohe PA, Painter S, Leary RF, Muhlfeld C, Allendorf FW, Luikart G. RAD sequencing yields a high success rate for westslope cutthroat and rainbow trout species-diagnostic SNP assays. Mol Ecol Res. 2012;12:653–60.Google Scholar
  5. Anderson EC. Assessing the power of informative subsets of loci for population assignment: standard methods are upwardly biased. Mol Ecol Res. 2010;10:701–10.Google Scholar
  6. Andrews KR, Luikart G. Recent novel approaches for population genomics data analysis. Mol Ecol. 2014;23:1661–7.PubMedGoogle Scholar
  7. Andrews KR, Good JM, Miller MR, Luikart G, Hohenlohe PA. Harnessing the power of RADseq for ecological and evolutionary genomics. Nat Rev Genet. 2016;17:81–92.PubMedPubMedCentralGoogle Scholar
  8. Avise JC. Molecular markers, natural history and evolution. New York: Chapman & Hall; 1994.Google Scholar
  9. Barrett CF, Bacon CD, Antonelli A, Cano A, Hofmann T. An introduction to plant phylogenomics with a focus on palms. Bot J Linn Soc. 2016;182:234–55.Google Scholar
  10. Bay RA, Harrigan RJ, Underwood VL, Gibbs HL, Smith TB, Ruegg K. Genomic signals of selection predict climate-driven population declines in a migratory bird. Science. 2018;359:83–6.PubMedGoogle Scholar
  11. Beaumont MA, Nichols RA. Evaluating loci for use in the genetic analysis of population structure. Proc R Soc B. 1996;263:1619–26.Google Scholar
  12. Benestan L, Gosselin T, Perrier C, Sainte-Marie B, Rochette R, Bernatchez L. RAD-genotyping reveals fine-scale genetic structuring and provides powerful population assignment in a widely distributed marine species; the American lobster (Homarus americanus). Mol Ecol. 2015;24:3299–315.PubMedGoogle Scholar
  13. Benestan LM, Ferchaud AL, Hohenlohe PA, Garner BA, Naylor GJP, Baums IB, et al. Conservation genomics of natural and managed populations: building a conceptual and practical framework. Mol Ecol. 2016;25:2967–77.PubMedGoogle Scholar
  14. Beraldi D, McRae AF, Gratten J, Slate J, Visscher PM, Pemberton JM. Mapping quantitative trait loci underlying fitness-related traits in a free-living sheep population. Evolution. 2007;61:1403–16.PubMedGoogle Scholar
  15. Bernatchez L. On the maintenance of genetic variation and adaptation to environmental change: considerations from population genomics in fishes. J Fish Biol. 2016;89:2519–56.Google Scholar
  16. Berthelot C, Brunet F, Chalopin D, Juanchich A, Bernard M, et al. The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun. 2014;5:3657.PubMedPubMedCentralGoogle Scholar
  17. Black WC, Baer CF, Antolin MF, DuTeau NM. Population genomics: genome-wide sampling of insect populations. Annu Rev Entomol. 2001;46:441–69.PubMedGoogle Scholar
  18. Boyer MC, Muhlfeld CC, Allendorf FW. Rainbow trout (Oncorhynchus mykiss) invasion and the spread of hybridization with native westslope cutthroat trout (Oncorhynchus clarkia lewisii). Can J Fish Aquat Sci. 2008;65:658–69.Google Scholar
  19. Bragg JG, Potter S, Bi K, Moritz C. Exon capture phylogenomics: efficacy across scales of divergence. Mol Ecol Resour. 2016;16:1059–68.PubMedGoogle Scholar
  20. Campbell NR, Harmon SA, Narum SR. Genotyping-in-thousands by sequencing (GT-seq): a cost effective SNP genotyping method based on custom amplicon sequencing. Mol Ecol Res. 2015;15:855–67.Google Scholar
  21. Catchen J, Hohenlohe PA, Bernatchez L, Funk WC, Andrews KR, Allendorf FW. Unbroken: RADseq remains a powerful tool for understanding the genetics of adaptation in natural populations. Mol Ecol Res. 2017;17:362–5.Google Scholar
  22. Chain FJJ, Feulner PGD, Panchal M, Eizaguirre C, Samonte IE, et al. Extensive copy-number variation of young genes across stickleback populations. PLoS Genet. 2014;10:e1004830.PubMedPubMedCentralGoogle Scholar
  23. Chan CX, Ragan MA. Next-generation phylogenomics. Biol Direct. 2013;8:3.PubMedPubMedCentralGoogle Scholar
  24. Cho YS, Hu L, Hou H, Lee H, Xu J, Kwon S, et al. The tiger genome and comparative analysis with lion and snow leopard genomes. Nat Commun. 2013;4:2433.PubMedPubMedCentralGoogle Scholar
  25. Coop G, Witonsky D, Di Rienzo A, Pritchard JK. Using environmental correlations to identify loci underlying local adaptation. Genetics. 2010;185:1411–23.PubMedPubMedCentralGoogle Scholar
  26. Corander J, Majander KK, Cheng L, Merila J. High degree of cryptic population differentiation in the Baltic Sea herring Clupea harengus. Mol Ecol. 2013;22:2931–40.PubMedGoogle Scholar
  27. Cornuet J-M, Pudlo P, Veyssier J, Dehne-Garcia A, Gautier M, Leblois R, et al. DIYABC v2.0: a software to make approximate Bayesian computation inferences about population history using single nucleotide polymorphism, DNA sequence and microsatellite data. Bioinformatics. 2014;30:1187–9.PubMedGoogle Scholar
  28. Cresko WA, Amores A, Wilson C, Murphy J, Currey M, Phillips P, Bell MA, Kimmel CB, Postlethwait JH. Parallel genetic basis for repeated evolution of armor loss in Alaskan threespine stickleback populations. Proc Natl Acad Sci U S A. 2004;101:6050–5.PubMedPubMedCentralGoogle Scholar
  29. Dawson E, Abecasis GR, Bumpstead S, Chen Y, Hunt S, Beare DM, et al. A first-generation linkage disequilibrium map of human chromosome 22. Nature. 2002;418:544–8.PubMedGoogle Scholar
  30. De Mita S, Thuillet A-C, Gay L, Ahmadi N, Manel S, Ronfort J, et al. Detecting selection along environmental gradients: analysis of eight methods and their effectiveness for outbreeding and selfing populations. Mol Ecol. 2013;22:1383–99.PubMedGoogle Scholar
  31. Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR. NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (N e) from genetic data. Mol Ecol Res. 2014;14:209–14.Google Scholar
  32. Dunning AM, Durocher F, Healey CS, Teare MD, McBride SE, Carlomagno F, et al. The extent of linkage disequilibrium in four populations with distinct demographic histories. Am J Human Genet. 2000;67:1544–54.Google Scholar
  33. Edwards SV, Potter S, Schmitt CJ, Bragg JG, Moritz C. Reticulation, divergence, and the phylogeography–phylogenetics continuum. Proc Natl Acad Sci. 2016;113:8025–32.PubMedGoogle Scholar
  34. Ekblom R, Galindo J. Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity. 2011;107(1):11.Google Scholar
  35. Elbers JP, Clostio RW, Taylor SS. Population genetic inferences using immune gene SNPs mirror patterns inferred by microsatellites. Mol Ecol Resour. 2017;17:481–91.PubMedGoogle Scholar
  36. Ellegren H, Smeds L, Burri R, Olason PI, Backström N, Kawakami T, et al. The genomic landscape of species divergence in Ficedula flycatchers. Nature. 2012;491:756–60.PubMedGoogle Scholar
  37. Emerson KJ, Merz CR, Catchen JM, Hohenlohe PA, Cresko WA, Bradshaw WE, et al. Resolving postglacial phylogeography using high-throughput sequencing. Proc Natl Acad Sci U S A. 2010;107:16196–200.PubMedPubMedCentralGoogle Scholar
  38. Epstein B, Jones M, Hamede R, Hendricks S, McCallum H, Murchison EP, et al. Rapid evolutionary response to a transmissible cancer in Tasmanian devils. Nat Commun. 2016;7:12684.PubMedPubMedCentralGoogle Scholar
  39. Ferchaud AL, Hansen MM. The impact of selection, gene flow and demographic history on heterogeneous genomic divergence: three-spine sticklebacks in divergent environments. Mol Ecol. 2016;25:238–59.PubMedGoogle Scholar
  40. Feulner PGD, Chain FJJ, Panchal M, Huang Y, Eizaguirre C, Kalbe M, et al. Genomics of divergence along a continuum of parapatric population differentiation. PLoS Genet. 2015;11:e1004966.PubMedPubMedCentralGoogle Scholar
  41. Fischer MC, Rellstab C, Leuzinger M, Roumet M, Gugerli F, Shimizu KK, et al. Estimating genomic diversity and population differentiation – an empirical comparison of microsatellite and SNP variation in Arabidopsis halleri. BMC Genomics. 2017;18:69.PubMedPubMedCentralGoogle Scholar
  42. Fisher RA. The genetic theory of natural selection. New York: Dover; 1958.Google Scholar
  43. Fontaine MC, Snirc A, Frantzis A, Koutrakis E, Öztürk B, Öztürk AA, Austerliz F. History of expansion and anthropogenic collapse in a top marine predator of the Black Sea estimated from genetic data. Proc Natl Acad Sci U S A. 2012;109:E2569–76.PubMedPubMedCentralGoogle Scholar
  44. Forester BR, Jones MR, Joost S, Landguth EL, Lasky JR. Detecting spatial genetic signatures of local adaptation in heterogeneous landscapes. Mol Ecol. 2016;25:104–20.PubMedGoogle Scholar
  45. Frichot E, Schoville SD, Bouchard G, François O. Testing for associations between loci and environmental gradients using latent factor mixed models. Mol Biol Evol. 2013;30:1687–99.PubMedPubMedCentralGoogle Scholar
  46. Fumagalli M, Sironi M, Pozzoli U, Ferrer-Admetlla A, Pattini L, et al. Signatures of environmental genetic adaptation pinpoint pathogens as the main selective pressure through human evolution. PLoS Genet. 2011;7:e1002355.PubMedPubMedCentralGoogle Scholar
  47. Funk WC, McKay JK, Hohenlohe PA, Allendorf FW. Harnessing genomics for delineating conservation units. Trends Ecol Evol. 2012;27:489–96.PubMedPubMedCentralGoogle Scholar
  48. Funk WC, Lovich RE, Hohenlohe PA, Hofman CA, Morrison SA, Sillett TS, et al. Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis). Mol Ecol. 2016;25:2176–94.PubMedPubMedCentralGoogle Scholar
  49. Garner BA, Hand BK, Amish SJ, Bernatchez L, Foster JT, Miller KM, et al. Genomics in conservation: case studies and bridging the gap between data and application. Trends Ecol Evol. 2015;31:81–2.PubMedGoogle Scholar
  50. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD. Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genet. 2009;5:e1000695.PubMedPubMedCentralGoogle Scholar
  51. Halverson A. An entirely synthetic fish: how rainbow trout beguiled America and overran the world. New Haven: Yale University Press; 2010.Google Scholar
  52. Hancock AM, Witonsky DB, Alkorta-Aranburu G, Beall CM, Gebremedhin A, Sukernik R, et al. Adaptations to climate-mediated selective pressures in humans. PLoS Genet. 2011;7:e1001375.PubMedPubMedCentralGoogle Scholar
  53. Hand BK, Hether TD, Kovach RP, Muhlfeld CC, Amish SJ, Boyer MC, O’Rourke SM, Miller MR, Lowe WH, Hohenlohe PA, Luikart G. Genomics and introgression: discovery and mapping of thousands of species-diagnostic SNPs using RAD sequencing. Curr Zool. 2015;61:146–54.Google Scholar
  54. Hand BK, Muhlfeld CC, Wade AA, Kovach RP, Whited DC, Narum SR, Matala AP, Ackerman MW, Garner BA, Kimball JS, Stanford JA, Luikart G. Climate variables explain neutral and adaptive variation within salmonid metapopulations: the importance of replication in landscape genetics. Mol Ecol. 2016;25:689–705.PubMedGoogle Scholar
  55. Hermisson J. Who believes in whole-genome scans for selection? Heredity. 2009;103:283–4.PubMedGoogle Scholar
  56. Herrera S, Shank TM. RAD sequencing enables unprecedented phylogenetic resolution and objective species delimitation in recalcitrant divergent taxa. Mol Phylogenet Evol. 2016;100:70–9.PubMedGoogle Scholar
  57. Hess JE, Campbell NR, Close DA, Docker MF, Narum SR. Population genomics of Pacific lamprey: adaptive variation in a highly dispersive species. Mol Ecol. 2013;22:2898–916.PubMedGoogle Scholar
  58. Hoban S, Kelley JL, Lotterhos KE, Antolin MF, Bradburd G, Lowry DB, et al. Finding the genomic basis of local adaptation: pitfalls, practical solutions, and future directions. Am Nat. 2016;188:379–97.PubMedPubMedCentralGoogle Scholar
  59. Hoffman JI, Simpson F, David P, Rijks JM, Kuiken T, Thorne MAS, et al. High-throughput sequencing reveals inbreeding depression in a natural population. Proc Natl Acad Sci U S A. 2014;111:3775–80.PubMedPubMedCentralGoogle Scholar
  60. Hohenlohe PA, Phillips PC, Cresko WA. Using population genomics to detect selection in natural populations: key concepts and methodological considerations. Int J Plant Sci. 2010;171:1059–71.PubMedPubMedCentralGoogle Scholar
  61. Hohenlohe PA, Amish SJ, Catchen JM, Allendorf FW, Luikart G. Next-generation RAD sequencing identified thousands of SNPs for assessing hybridization between rainbow and westslope cutthroat trout. Mol Ecol Res. 2011;11:117–22.Google Scholar
  62. Hohenlohe PA, Day MD, Amish SJ, Miller MR, Kamps-Hughes N, Boyer MC, Muhlfeld CC, Allendorf FW, Johnson EA, Luikart G. Genomic patterns of introgression in rainbow and westslope cutthroat trout illuminated by overlapping paired-end RAD sequencing. Mol Ecol. 2013;22:3002–13.PubMedPubMedCentralGoogle Scholar
  63. Holliday JA, Hallerman EM, Haak DC. Genotyping and sequencing technologies in population genetics and genomics. Cham: Springer; 2018.Google Scholar
  64. Jarvis ED. Perspectives from the avian phylogenomics project: questions that can be answered with sequencing all genomes of a vertebrate class. Annu Rev Anim Biosci. 2016;4:45–59.PubMedGoogle Scholar
  65. Jeffries DL, Copp GH, Lawson Handley L, Olsén KH, Sayer CD, Hänfling B. Comparing RADseq and microsatellites to infer complex phylogeographic patterns, an empirical perspective in the Crucian carp, Carassius carassius, L. Mol Ecol. 2016;25:2997–3018.PubMedGoogle Scholar
  66. Jones MR, Good JM. Targeted capture in evolutionary and ecological genomics. Mol Ecol. 2016;25:185–202.PubMedGoogle Scholar
  67. Jones FC, Grabherr MG, Chan YF, Russell P, Maucell E, Johnson J. The genomic basis of adaptive evolution in threespine sticklebacks. Nature. 2012;484:55–61.PubMedPubMedCentralGoogle Scholar
  68. Joost S, Bonin A, Bruford W, Després CC, Erhardt G, Taberlet P. A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation. Mol Ecol. 2007;16:3955–69.PubMedGoogle Scholar
  69. Kaiser SA, Taylor SA, Chen N, Sillett TS, Bondra ER, Webster MS. A comparative assessment of SNP and microsatellite markers for assigning parentage in a socially monogamous bird. Mol Ecol Resour. 2016;17:183–93.PubMedGoogle Scholar
  70. Kardos M, Luikart G, Allendorf FW. Measuring individual inbreeding in the age of genomics: marker-based measures are better than pedigrees. Heredity. 2015;115:63–72.PubMedPubMedCentralGoogle Scholar
  71. Kardos M, Taylor HR, Ellegren H, Luikart G, Allendorf FW. Genomics advances the study of inbreeding depression in the wild. Evol Appl. 2016;9:1205–18.PubMedPubMedCentralGoogle Scholar
  72. Keller I, Wagner CE, Greuter L, Mwaiko S, Selz OM, Sivasundar A, et al. Population genomic signatures of divergent adaptation, gene flow and hybrid speciation in the rapid radiation of Lake Victoria cichlid fishes. Mol Ecol. 2013;22:2848–63.PubMedGoogle Scholar
  73. Kimura M. The neutral theory of molecular evolution. Cambridge: Cambridge University Press; 1983.Google Scholar
  74. Kovach RP, Muhlfeld CC, Boyer MC, Lowe WH, Allendorf FW, Luikart G. Dispersal and selection mediate hybridization between a native and invasive species. Proc R Soc B. 2015;282:20142454.PubMedGoogle Scholar
  75. Kovach RP, Hand BK, Hohenlohe PA, Cosart TF, Boyer MC, Neville HH, Muhlfeld CC, Amish SJ, Carim K, Narum SR, Lowe WH, Allendorf FW, Luikart G. Vive la résistance: genome-wide selection against introduced alleles in invasive hybrid zones. Proc R Soc B. 2016;283:20161380.PubMedGoogle Scholar
  76. Landguth EL, Balkenhol N. Relative sensitivity of neutral versus adaptive genetic data for assessing population differentiation. Conserv Genet. 2012;13:1421–6.Google Scholar
  77. Larson WA, Seeb LW, Everett MV, Waples RK, Templin WD, Seeb JE. Genotyping by sequencing resolves shallow population structure to inform conservation of Chinook salmon (Oncorhynchus tshawytscha). Evol Appl. 2014;7:355–69.PubMedPubMedCentralGoogle Scholar
  78. Leaché AD, Chavez AS, Jones LN, Grummer JA, Gottscho AD, Linkem CW. Phylogenomics of Phrynosomatid lizards: conflicting signals from sequence capture versus restriction site associated DNA sequencing. Genome Biol Evol. 2015;7:706–19.PubMedPubMedCentralGoogle Scholar
  79. LeCorre V, Kremer A. The genetic differentiation at quantitative trait loci under local adaptation. Mol Ecol. 2012;21:1548–66.Google Scholar
  80. Leroy T, Roux C, Villate L, Boldénès C, Romiguier J, Paiva JAP, et al. Extensive recent secondary contacts between four European white oak species. New Phytol. 2017;214:865–78.PubMedPubMedCentralGoogle Scholar
  81. Lewontin RC. Genetic basis of evolutionary change. New York: Columbia University Press; 1974.Google Scholar
  82. Lewontin RC, Krakauer J. Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics. 1973;74:175–95.PubMedPubMedCentralGoogle Scholar
  83. Li H, Durbin R. Inference of human population history from individual whole-genome sequences. Nat Genet. 2011;475:493–6.Google Scholar
  84. Limborg MT, Helyar SJ, DeBruyn M, Taylor MI, Nielsen EE, Ogden R, Carvalho GR, Bekkevold D. Environmental selection on transcriptome-derived SNPs in a high gene flow marine fish, the Atlantic herring (Clupea harengus). Mol Ecol. 2012;21:3686–703.PubMedGoogle Scholar
  85. Lind BM, Friedline CJ, Wegrzyn JL, Maloney PE, Vogler DR, Neale DB, Eckert AJ. Water availability drives signatures of local adaptation in whitebark pine (Pinus albicaulis Engelm.) across fine spatial scales of the Lake Tahoe Basin, USA. Mol Ecol. 2017;26:3168–85.PubMedGoogle Scholar
  86. Linløkken AN, Haugen TO, Mathew PK, Johansen W, Lien S. Comparing estimates of number of breeders Nb based on microsatellites and single nucleotide polymorphism of three groups of brown trout (Salmo trutta L.). Fish Manag Ecol. 2016;23:152–60.Google Scholar
  87. Liu J, Shikano T, Leinonen T, Cano JM, Li M-H, Merilä J. Identification of major and minor QTL for ecologically important morphological traits in three-spined sticklebacks (Gasterosteus aculeatus). G3 Genes Genomes Genet. 2014;4:595–604.Google Scholar
  88. Loh P-R, Lipson M, Patterson N, Moorjani P, Pickrell JK, Reich D, Berger B. Inferring admixture histories of human populations using linkage disequilibrium. Genetics. 2013;193:1233–48.PubMedPubMedCentralGoogle Scholar
  89. Lowry DB, Hoban S, Kelley JL, Lotterhos KE, Reed LK, Antolin MF, et al. Breaking RAD: an evaluation of the utility of restriction site associated DNA sequencing for genome scans of adaptation. Mol Ecol Resour. 2016;17:142–52.PubMedPubMedCentralGoogle Scholar
  90. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P. The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet. 2003;4:981–94.PubMedGoogle Scholar
  91. Luikart G, Kardos M, Hand BK, Rajora OP, Aitken SN, Hohenlohe PA. Population genomics. Cham: Springer; 2018.Google Scholar
  92. Malenfant R, Coltman DW, Davis CS. Design of a 9K Illumina BeadChip for polar bears (Ursus maritimus) from RAD and transcriptome sequencing. Mol Ecol Resour. 2015;15:587–600.PubMedGoogle Scholar
  93. Mardis ER. The impact of next-generation sequencing technology on genetics. Trends Genet. 2008;24:133–41.PubMedGoogle Scholar
  94. Matala AP, Ackerman MW, Campbell MR, Narum SR. Relative contributions of neutral and non-neutral genetic differentiation to inform conservation of steelhead trout across highly variable landscapes. Evol Appl. 2014;7:682–701.PubMedPubMedCentralGoogle Scholar
  95. Mazet O, Rodríguez W, Grusea S, Boitard S, Chikhi L. On the importance of being structured: instantaneous coalescence rates and a re-evaluation of human evolution. Heredity. 2016;116:362–71.PubMedGoogle Scholar
  96. McCartney-Melstad E, Mount GG, Shaffer HB. Exon capture optimization in amphibians with large genomes. Mol Ecol. 2016;16:1084–94.Google Scholar
  97. McCormack JE, Hird SM, Zellmer AJ, Carstens BC, Brumfield RT. Applications of next-generation sequencing to phylogeography and phylogenetics. Mol Phylogenet Evol. 2013;66:526–38.PubMedGoogle Scholar
  98. Mckinney GJ, Larson WA, Seeb LW, Seeb JE. RADseq provides unprecedented insights into molecular ecology and evolutionary genetics: comment on breaking RAD by Lowry et al. (2016). Mol Ecol Resour. 2017;17:356–61.PubMedGoogle Scholar
  99. McManus KF, Kelley JL, Song S, Veeramah KR, Woerner AE, Stevison LS, et al. Inference of gorilla demographic and selective history from whole-genome sequence data. Mol Biol Evol. 2016;32:600–12.Google Scholar
  100. Milano I, Babbucci M, Cariani A, Atanassova M, Bekkevold D, Carvalho GR, et al. Outlier SNP markers reveal fine-scale genetic structuring across European hake populations (Merluccius merluccius). Mol Ecol. 2014;23:118–35.PubMedGoogle Scholar
  101. Miller MR, Brunelli JP, Wheeler PA, Liu S, Rexroad CE, Palti Y, et al. A conserved haplotype controls parallel adaptation in geographically distant salmonid populations. Mol Ecol. 2012;21:237–49.PubMedPubMedCentralGoogle Scholar
  102. Morin PA, Parsons KM, Archer FI, Ávila-Arcos MC, Barrett-Lennard LG, Dalla Rosa L, et al. Geographic and temporal dynamics of a global radiation and diversification in the killer whale. Mol Ecol. 2015;24:3964–79.PubMedGoogle Scholar
  103. Moritz C, Hillis DM. Molecular systematics: context and controversies. In: Hillis DM, Moritz C, Mable BK, editors. Molecular systematics. 2nd ed. Sunderland: Sinauer; 1996. p. 1–16.Google Scholar
  104. Moura AE, Kenny JG, Chaudhuri R, Hughes MA, Welch AJ, Reisinger RR, et al. Population genomics of the killer whale indicates ecotype evolution in sympatry involving both selection and drift. Mol Ecol. 2014;23:5179–92.PubMedPubMedCentralGoogle Scholar
  105. Muhlfeld CC, Kalinowski ST, McMahon TE, Taper ML, Painter S, Leary RF, Allendorf FW. Hybridization rapidly reduces fitness of a native trout in the wild. Biol Lett. 2009;5:328–31.PubMedPubMedCentralGoogle Scholar
  106. Muhlfeld CC, Kovach RP, Jones LA, Al-Chokhachy R, Boyer MC, Leary RF, et al. Invasive hybridization in a threatened species is accelerated by climate change. Nat Clim Change. 2014;4:620–4.Google Scholar
  107. Mullis KB, Faloona FA. Specific synthesis of DNA in vitro via a polymerase-catalyzed chain reaction. Methods Enzymol. 1987;155:335–50.PubMedGoogle Scholar
  108. Nadachowska-Brzyska K, Burri R, Smeds L, Ellegren H. PSMC analysis of effective population sizes in molecular ecology and its application to black-and-white Ficedula flycatchers. Mol Ecol. 2016;25:1058–72.PubMedPubMedCentralGoogle Scholar
  109. Nadeau NJ, Ruiz M, Salazar P, Counterman B, Medina JA, Ortiz-Zuazaga H, et al. Population genomics of parallel hybrid zones in the mimetic butterflies, H. melpomene and H. erato. Genome Res. 2014;24:1316–33.PubMedPubMedCentralGoogle Scholar
  110. Nazareno AG, Bemmels JB, Dick CW, Lohmann LG. Minimum sample sizes for population genomics: an empirical study from an Amazonian plant species. Mol Ecol Resour. 2017;17:1136–47.PubMedGoogle Scholar
  111. Nicolle D. A classification and census of regenerative strategies in the eucalypts (Angophora, Corymbia and Eucalyptus – Myrtaceae), with special reference to the obligate seeders. Aust J Bot. 2006;54:391–407.Google Scholar
  112. Oswald JA, Overcast I, Mauck WM, Anderson MJ, Smith BT. Isolation with asymmetric gene flow during the nonsynchronous divergence of dry forest birds. Mol Ecol. 2017;26:1386–400.PubMedGoogle Scholar
  113. Palsbøll PJ, Bérubé M, Allendorf FW. Identification of management units using population genetic data. Trends Ecol Evol. 2007;22:11–6.PubMedGoogle Scholar
  114. Park L. Effective population size of current human population. Genet Res. 2011;93:105–14.Google Scholar
  115. Pickrell JK, Pritchard JK. Inference of population splits and mixtures from genome-wide allele frequency data. PLoS Genet. 2012;8:e1002967.PubMedPubMedCentralGoogle Scholar
  116. Puckett EE, Eggert LS. Comparison of SNP and microsatellite genotyping panels for spatial assignment of individuals to natal range: a case study using the American black bear (Ursus americanus). Biol Conserv. 2016;193:86–93.Google Scholar
  117. Rajora OP, Eckert AJ, Zinck JWR. Single-locus versus multilocus patterns of local adaptation to climate in eastern white pine (Pinus strobus, Pinaceae). PLoS One. 2016;11:e0158691.PubMedPubMedCentralGoogle Scholar
  118. Ree RH, Hipp AL. Inferring phylogenetic history from restriction site associated DNA (RADseq). In: Hörandl E, Appelhans MS, editors. Next-generation sequencing in plant systematics. Königstein: International Association for Plant Taxonomy, IAPT; 2015. p. 1–24.Google Scholar
  119. Reich DE, Cargill M, Bolk S, Ireland J, Sabeti PC, Richter DJ, et al. Linkage disequilibrium in the human genome. Nature. 2001;411:199–204.PubMedGoogle Scholar
  120. Rellstab C, Gugerli F, Eckert AJ, Hancock AM, Holderegger R. A practical guide to environmental association analysis in landscape genomics. Mol Ecol. 2015;24:4348–70.PubMedGoogle Scholar
  121. Robinson JA, Ortega-Del Vecchyo D, Fan Z, Kim BY, Vonholdt BM, Marsden CD, et al. Genomic flatlining in the endangered island fox. Curr Biol. 2016;26(9):1183.PubMedGoogle Scholar
  122. Rougement Q, Gagnaire P-A, Perrier C, Genthon C, Besnard A-L, Launey S, Evanno G. Inferring the demographic history underlying parallel genomic divergence among pairs of parasitic and nonparasitic lamprey ecotypes. Mol Ecol. 2016;26:142–62.Google Scholar
  123. Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977;74:5463–7.PubMedPubMedCentralGoogle Scholar
  124. Sansaloni C, Petroli C, Jaccoud D, Carling J, Detering F, Grattapaglia D, et al. Diversity Arrays Technology (DArT) and next-generation sequencing combined: genome-wide, high throughput, highly informative genotyping for molecular breeding of Eucalyptus. BMC Proc. 2011;5:P54.PubMedCentralGoogle Scholar
  125. Santure AW, De Cauwer I, Robinson MR, Poissant J, Sheldon BC, Slate J. Genomic dissection of variation in clutch size and egg mass in a wild great tit (Parus major) population. Mol Ecol. 2013;22:3949–62.PubMedGoogle Scholar
  126. Schield DR, Adams RH, Card DC, Perry BW, Pasquesi GM, Jezkova T, et al. Insight into the roles of selection in speciation from genomic patterns of divergence and introgression in secondary contact in venomous rattlesnakes. Ecol Evol. 2017;7:3951–66.PubMedPubMedCentralGoogle Scholar
  127. Schoville SD, Bonin A, François O, Lobreaux S, Melodelima C, Manel S. Adaptive genetic variation on the landscape: methods and cases. Annu Rev Ecol Evol Syst. 2012;43:23–43.Google Scholar
  128. Selkoe KA, Toonen RJ. Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett. 2006;9:615–29.PubMedGoogle Scholar
  129. Slate J, Visscher PM, MacGregor S, Stevens D, Tate ML, Pemberton JM. A genome scan for quantitative trait loci in a wild population of red deer (Cervus elaphus). Genetics. 2002;162:1863–73.PubMedPubMedCentralGoogle Scholar
  130. Spurgin LG, Wright DJ, van der Velde M, Collar NJ, Komdeur J, Burke T, Richardson DS. Museum DNA reveals the demographic history of the endangered Seychelles warbler. Evol Appl. 2014;7:1134–43.PubMedPubMedCentralGoogle Scholar
  131. Steane DA, Potts BM, McLean E, Prober SM, Stock WD, Vaillancourt RE, et al. Genome-wide scans detect adaptation to aridity in a widespread forest tree species. Mol Ecol. 2014;23:2500–13.PubMedGoogle Scholar
  132. Steane DA, Potts BM, McLean E, Collins L, Prober SM, Stock WD, Vaillancourt RE, Byrne M. Genome-wide scans reveal cryptic population structure in a dry-adapted eucalypt. Tree Genet Genomes. 2015;11:33.Google Scholar
  133. Terhorst J, Kamm JA, Song YS. Robust and scalable inference of population history from hundreds of unphased whole genomes. Nat Genet. 2017;49:303–9.PubMedGoogle Scholar
  134. Therkildsen NO, Palumbi SR. Practical low-coverage genomewide sequencing of hundreds of individually barcoded samples for population and evolutionary genomics in nonmodel species. Mol Ecol Resour. 2017;17:194–208.PubMedGoogle Scholar
  135. Tiffin P, Ross-Ibarra J. Advances and limits of using population genetics to understand local adaptation. Trends Ecol Evol. 2014;29:673–80.PubMedGoogle Scholar
  136. Vargas OM, Ortiz EM, Simpson BB. Conflicting phylogenomic signals reveal a pattern of reticulate evolution in a recent high-Andean diversification (Asteraceae: Astereae: Diplostephium). New Phytol. 2017;214:1736–50.PubMedGoogle Scholar
  137. Wagner CE, Keller I, Wittwer S, Selz OM, Mwaiko S, Greuter L, et al. Genome-wide RAD sequence data provide unprecedented resolution of species boundaries and relationships in the Lake Victoria cichlid adaptive radiation. Mol Ecol. 2013;22:787–98.PubMedGoogle Scholar
  138. Wang Z, Gerstein M, Snyder M. RNA-seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 2009;10:57–63.PubMedPubMedCentralGoogle Scholar
  139. White TA, Perkins SE, Heckel G, Searle JB. Adaptive evolution during an ongoing range expansion: the invasive bank vole (Myodes glareolus) in Ireland. Mol Ecol. 2013;22:2971–85.PubMedGoogle Scholar
  140. Whitlock MC, Lotterhos KE. Reliable detection of loci responsible for local adaptation: inference of a null model through trimming the distribution of F ST. Am Nat. 2015;186:S24–36.PubMedGoogle Scholar
  141. Wright S. Evolution and the genetics of populations. Chicago: University of Chicago Press; 1978.Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Paul A. Hohenlohe
    • 1
    Email author
  • Brian K. Hand
    • 2
  • Kimberly R. Andrews
    • 3
    • 4
  • Gordon Luikart
    • 2
  1. 1.Department of Biological SciencesInstitute for Bioinformatics and Evolutionary Studies, University of IdahoMoscowUSA
  2. 2.Flathead Lake Biological Station, Conservation Genomics Group, Division of Biological SciencesUniversity of MontanaPolsonUSA
  3. 3.Department of Fish and Wildlife SciencesUniversity of IdahoMoscowUSA
  4. 4.Genetics and Genomics Group, NOAA Pacific Marine Environmental LabUniversity of Washington JISAOSeattleUSA

Personalised recommendations